Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in <italic toggle="yes"<Rhizobiales</italic<

ABSTRACT Members of the order Rhizobiales include those capable of nitrogen fixation in nodules as well as pathogens of animals and plants. This lifestyle diversity has important implications for agricultural and medical research. Leveraging large-scale genomic data, we infer that Rhizobiales originated as a free-living ancestor ∼1,500 million years ago (Mya) and that the later emergence of host-associated lifestyles broadly coincided with the rise of their eukaryotic hosts. In particular, the first nodulating lineage arose from either Azorhizobium or Bradyrhizobium 150 to 80 Mya, a time range in general concurrent with the emergence of legumes. The rates of lifestyle transitions are highly variable; nodule association is more likely to be lost than gained, whereas animal association likely represents an evolutionary dead end. We searched for statistical correlations between gene presence and lifestyle and identified genes likely contributing to the transition and adaptation to the same lifestyle in divergent lineages. Among the genes potentially promoting successful transitions to major nodulation lineages, the nod and nif clusters for nodulation and nitrogen fixation, respectively, were repeatedly acquired during each transition; the fix, dct, and phb clusters involved in energy conservation under micro-oxic conditions were present in the nonnodulating ancestors; and the secretion systems were acquired in lineage-specific patterns. Our study data suggest that increased eukaryote diversity drives lifestyle diversification of bacteria and highlight both acquired and preexisting traits facilitating the origin of host association. IMPORTANCE Bacteria form diverse interactions with eukaryotic hosts. This is well represented by the Rhizobiales, a clade of Alphaproteobacteria strategically important for their large diversity of lifestyles with implications for agricultural and medical research. To investigate their lifestyle evolution, we compiled a comprehensive data set of genomes and lifestyle information for over 1,000 Rhizobiales genomes. We show that the origins of major host-associated lineages in Rhizobiales broadly coincided with the emergences of their host plants/animals, suggesting bacterium-host interactions as a driving force in the evolution of Rhizobiales. We further found that, in addition to gene gains, preexisting traits and recurrent losses of specific genomic traits may have played underrecognized roles in the origin of host-associated lineages, providing clues to genetic engineering of microbial agricultural inoculants and prevention of the emergence of potential plant/animal pathogens. Ausführliche Beschreibung

Gespeichert in:

Autor*in:	Sishuo Wang [verfasserIn] Andrew Meade [verfasserIn] Hon-Ming Lam [verfasserIn] Haiwei Luo [verfasserIn]

Format:	E-Artikel
Sprache:	Englisch

Erschienen:	2020

Schlagwörter:	Rhizobiales rhizobia lifestyle evolution molecular clock bacterial evolution microbial evolution

Übergeordnetes Werk:	In: mSystems - American Society for Microbiology, 2017, 5(2020), 4
Übergeordnetes Werk:	volume:5 ; year:2020 ; number:4

Links:	Link aufrufen Link aufrufen Link aufrufen Journal toc

DOI / URN:	10.1128/mSystems.00438-20

Katalog-ID:	DOAJ052384446

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allfields	10.1128/mSystems.00438-20 doi (DE-627)DOAJ052384446 (DE-599)DOAJ7a25dae7c7a0461eb78b81f6d46aa8bd DE-627 ger DE-627 rakwb eng QR1-502 Sishuo Wang verfasserin aut Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in <italic toggle="yes"<Rhizobiales</italic< 2020 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Members of the order Rhizobiales include those capable of nitrogen fixation in nodules as well as pathogens of animals and plants. This lifestyle diversity has important implications for agricultural and medical research. Leveraging large-scale genomic data, we infer that Rhizobiales originated as a free-living ancestor ∼1,500 million years ago (Mya) and that the later emergence of host-associated lifestyles broadly coincided with the rise of their eukaryotic hosts. In particular, the first nodulating lineage arose from either Azorhizobium or Bradyrhizobium 150 to 80 Mya, a time range in general concurrent with the emergence of legumes. The rates of lifestyle transitions are highly variable; nodule association is more likely to be lost than gained, whereas animal association likely represents an evolutionary dead end. We searched for statistical correlations between gene presence and lifestyle and identified genes likely contributing to the transition and adaptation to the same lifestyle in divergent lineages. Among the genes potentially promoting successful transitions to major nodulation lineages, the nod and nif clusters for nodulation and nitrogen fixation, respectively, were repeatedly acquired during each transition; the fix, dct, and phb clusters involved in energy conservation under micro-oxic conditions were present in the nonnodulating ancestors; and the secretion systems were acquired in lineage-specific patterns. Our study data suggest that increased eukaryote diversity drives lifestyle diversification of bacteria and highlight both acquired and preexisting traits facilitating the origin of host association. IMPORTANCE Bacteria form diverse interactions with eukaryotic hosts. This is well represented by the Rhizobiales, a clade of Alphaproteobacteria strategically important for their large diversity of lifestyles with implications for agricultural and medical research. To investigate their lifestyle evolution, we compiled a comprehensive data set of genomes and lifestyle information for over 1,000 Rhizobiales genomes. We show that the origins of major host-associated lineages in Rhizobiales broadly coincided with the emergences of their host plants/animals, suggesting bacterium-host interactions as a driving force in the evolution of Rhizobiales. We further found that, in addition to gene gains, preexisting traits and recurrent losses of specific genomic traits may have played underrecognized roles in the origin of host-associated lineages, providing clues to genetic engineering of microbial agricultural inoculants and prevention of the emergence of potential plant/animal pathogens. Rhizobiales rhizobia lifestyle evolution molecular clock bacterial evolution microbial evolution Microbiology Andrew Meade verfasserin aut Hon-Ming Lam verfasserin aut Haiwei Luo verfasserin aut In mSystems American Society for Microbiology, 2017 5(2020), 4 (DE-627)84597212X (DE-600)2844333-0 23795077 nnns volume:5 year:2020 number:4 https://doi.org/10.1128/mSystems.00438-20 kostenfrei https://doaj.org/article/7a25dae7c7a0461eb78b81f6d46aa8bd kostenfrei https://journals.asm.org/doi/10.1128/mSystems.00438-20 kostenfrei https://doaj.org/toc/2379-5077 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 5 2020 4
spelling	10.1128/mSystems.00438-20 doi (DE-627)DOAJ052384446 (DE-599)DOAJ7a25dae7c7a0461eb78b81f6d46aa8bd DE-627 ger DE-627 rakwb eng QR1-502 Sishuo Wang verfasserin aut Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in <italic toggle="yes"<Rhizobiales</italic< 2020 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Members of the order Rhizobiales include those capable of nitrogen fixation in nodules as well as pathogens of animals and plants. This lifestyle diversity has important implications for agricultural and medical research. Leveraging large-scale genomic data, we infer that Rhizobiales originated as a free-living ancestor ∼1,500 million years ago (Mya) and that the later emergence of host-associated lifestyles broadly coincided with the rise of their eukaryotic hosts. In particular, the first nodulating lineage arose from either Azorhizobium or Bradyrhizobium 150 to 80 Mya, a time range in general concurrent with the emergence of legumes. The rates of lifestyle transitions are highly variable; nodule association is more likely to be lost than gained, whereas animal association likely represents an evolutionary dead end. We searched for statistical correlations between gene presence and lifestyle and identified genes likely contributing to the transition and adaptation to the same lifestyle in divergent lineages. Among the genes potentially promoting successful transitions to major nodulation lineages, the nod and nif clusters for nodulation and nitrogen fixation, respectively, were repeatedly acquired during each transition; the fix, dct, and phb clusters involved in energy conservation under micro-oxic conditions were present in the nonnodulating ancestors; and the secretion systems were acquired in lineage-specific patterns. Our study data suggest that increased eukaryote diversity drives lifestyle diversification of bacteria and highlight both acquired and preexisting traits facilitating the origin of host association. IMPORTANCE Bacteria form diverse interactions with eukaryotic hosts. This is well represented by the Rhizobiales, a clade of Alphaproteobacteria strategically important for their large diversity of lifestyles with implications for agricultural and medical research. To investigate their lifestyle evolution, we compiled a comprehensive data set of genomes and lifestyle information for over 1,000 Rhizobiales genomes. We show that the origins of major host-associated lineages in Rhizobiales broadly coincided with the emergences of their host plants/animals, suggesting bacterium-host interactions as a driving force in the evolution of Rhizobiales. We further found that, in addition to gene gains, preexisting traits and recurrent losses of specific genomic traits may have played underrecognized roles in the origin of host-associated lineages, providing clues to genetic engineering of microbial agricultural inoculants and prevention of the emergence of potential plant/animal pathogens. Rhizobiales rhizobia lifestyle evolution molecular clock bacterial evolution microbial evolution Microbiology Andrew Meade verfasserin aut Hon-Ming Lam verfasserin aut Haiwei Luo verfasserin aut In mSystems American Society for Microbiology, 2017 5(2020), 4 (DE-627)84597212X (DE-600)2844333-0 23795077 nnns volume:5 year:2020 number:4 https://doi.org/10.1128/mSystems.00438-20 kostenfrei https://doaj.org/article/7a25dae7c7a0461eb78b81f6d46aa8bd kostenfrei https://journals.asm.org/doi/10.1128/mSystems.00438-20 kostenfrei https://doaj.org/toc/2379-5077 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 5 2020 4
allfields_unstemmed	10.1128/mSystems.00438-20 doi (DE-627)DOAJ052384446 (DE-599)DOAJ7a25dae7c7a0461eb78b81f6d46aa8bd DE-627 ger DE-627 rakwb eng QR1-502 Sishuo Wang verfasserin aut Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in <italic toggle="yes"<Rhizobiales</italic< 2020 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Members of the order Rhizobiales include those capable of nitrogen fixation in nodules as well as pathogens of animals and plants. This lifestyle diversity has important implications for agricultural and medical research. Leveraging large-scale genomic data, we infer that Rhizobiales originated as a free-living ancestor ∼1,500 million years ago (Mya) and that the later emergence of host-associated lifestyles broadly coincided with the rise of their eukaryotic hosts. In particular, the first nodulating lineage arose from either Azorhizobium or Bradyrhizobium 150 to 80 Mya, a time range in general concurrent with the emergence of legumes. The rates of lifestyle transitions are highly variable; nodule association is more likely to be lost than gained, whereas animal association likely represents an evolutionary dead end. We searched for statistical correlations between gene presence and lifestyle and identified genes likely contributing to the transition and adaptation to the same lifestyle in divergent lineages. Among the genes potentially promoting successful transitions to major nodulation lineages, the nod and nif clusters for nodulation and nitrogen fixation, respectively, were repeatedly acquired during each transition; the fix, dct, and phb clusters involved in energy conservation under micro-oxic conditions were present in the nonnodulating ancestors; and the secretion systems were acquired in lineage-specific patterns. Our study data suggest that increased eukaryote diversity drives lifestyle diversification of bacteria and highlight both acquired and preexisting traits facilitating the origin of host association. IMPORTANCE Bacteria form diverse interactions with eukaryotic hosts. This is well represented by the Rhizobiales, a clade of Alphaproteobacteria strategically important for their large diversity of lifestyles with implications for agricultural and medical research. To investigate their lifestyle evolution, we compiled a comprehensive data set of genomes and lifestyle information for over 1,000 Rhizobiales genomes. We show that the origins of major host-associated lineages in Rhizobiales broadly coincided with the emergences of their host plants/animals, suggesting bacterium-host interactions as a driving force in the evolution of Rhizobiales. We further found that, in addition to gene gains, preexisting traits and recurrent losses of specific genomic traits may have played underrecognized roles in the origin of host-associated lineages, providing clues to genetic engineering of microbial agricultural inoculants and prevention of the emergence of potential plant/animal pathogens. Rhizobiales rhizobia lifestyle evolution molecular clock bacterial evolution microbial evolution Microbiology Andrew Meade verfasserin aut Hon-Ming Lam verfasserin aut Haiwei Luo verfasserin aut In mSystems American Society for Microbiology, 2017 5(2020), 4 (DE-627)84597212X (DE-600)2844333-0 23795077 nnns volume:5 year:2020 number:4 https://doi.org/10.1128/mSystems.00438-20 kostenfrei https://doaj.org/article/7a25dae7c7a0461eb78b81f6d46aa8bd kostenfrei https://journals.asm.org/doi/10.1128/mSystems.00438-20 kostenfrei https://doaj.org/toc/2379-5077 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 5 2020 4
allfieldsGer	10.1128/mSystems.00438-20 doi (DE-627)DOAJ052384446 (DE-599)DOAJ7a25dae7c7a0461eb78b81f6d46aa8bd DE-627 ger DE-627 rakwb eng QR1-502 Sishuo Wang verfasserin aut Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in <italic toggle="yes"<Rhizobiales</italic< 2020 Text txt rdacontent Computermedien c rdamedia Online-Ressource cr rdacarrier ABSTRACT Members of the order Rhizobiales include those capable of nitrogen fixation in nodules as well as pathogens of animals and plants. This lifestyle diversity has important implications for agricultural and medical research. Leveraging large-scale genomic data, we infer that Rhizobiales originated as a free-living ancestor ∼1,500 million years ago (Mya) and that the later emergence of host-associated lifestyles broadly coincided with the rise of their eukaryotic hosts. In particular, the first nodulating lineage arose from either Azorhizobium or Bradyrhizobium 150 to 80 Mya, a time range in general concurrent with the emergence of legumes. The rates of lifestyle transitions are highly variable; nodule association is more likely to be lost than gained, whereas animal association likely represents an evolutionary dead end. We searched for statistical correlations between gene presence and lifestyle and identified genes likely contributing to the transition and adaptation to the same lifestyle in divergent lineages. Among the genes potentially promoting successful transitions to major nodulation lineages, the nod and nif clusters for nodulation and nitrogen fixation, respectively, were repeatedly acquired during each transition; the fix, dct, and phb clusters involved in energy conservation under micro-oxic conditions were present in the nonnodulating ancestors; and the secretion systems were acquired in lineage-specific patterns. Our study data suggest that increased eukaryote diversity drives lifestyle diversification of bacteria and highlight both acquired and preexisting traits facilitating the origin of host association. IMPORTANCE Bacteria form diverse interactions with eukaryotic hosts. This is well represented by the Rhizobiales, a clade of Alphaproteobacteria strategically important for their large diversity of lifestyles with implications for agricultural and medical research. To investigate their lifestyle evolution, we compiled a comprehensive data set of genomes and lifestyle information for over 1,000 Rhizobiales genomes. We show that the origins of major host-associated lineages in Rhizobiales broadly coincided with the emergences of their host plants/animals, suggesting bacterium-host interactions as a driving force in the evolution of Rhizobiales. We further found that, in addition to gene gains, preexisting traits and recurrent losses of specific genomic traits may have played underrecognized roles in the origin of host-associated lineages, providing clues to genetic engineering of microbial agricultural inoculants and prevention of the emergence of potential plant/animal pathogens. Rhizobiales rhizobia lifestyle evolution molecular clock bacterial evolution microbial evolution Microbiology Andrew Meade verfasserin aut Hon-Ming Lam verfasserin aut Haiwei Luo verfasserin aut In mSystems American Society for Microbiology, 2017 5(2020), 4 (DE-627)84597212X (DE-600)2844333-0 23795077 nnns volume:5 year:2020 number:4 https://doi.org/10.1128/mSystems.00438-20 kostenfrei https://doaj.org/article/7a25dae7c7a0461eb78b81f6d46aa8bd kostenfrei https://journals.asm.org/doi/10.1128/mSystems.00438-20 kostenfrei https://doaj.org/toc/2379-5077 Journal toc kostenfrei GBV_USEFLAG_A SYSFLAG_A GBV_DOAJ GBV_ILN_20 GBV_ILN_22 GBV_ILN_23 GBV_ILN_24 GBV_ILN_39 GBV_ILN_40 GBV_ILN_62 GBV_ILN_63 GBV_ILN_65 GBV_ILN_69 GBV_ILN_70 GBV_ILN_73 GBV_ILN_74 GBV_ILN_95 GBV_ILN_105 GBV_ILN_110 GBV_ILN_151 GBV_ILN_161 GBV_ILN_170 GBV_ILN_213 GBV_ILN_230 GBV_ILN_285 GBV_ILN_293 GBV_ILN_602 GBV_ILN_2014 GBV_ILN_4012 GBV_ILN_4037 GBV_ILN_4112 GBV_ILN_4125 GBV_ILN_4126 GBV_ILN_4249 GBV_ILN_4305 GBV_ILN_4306 GBV_ILN_4307 GBV_ILN_4313 GBV_ILN_4322 GBV_ILN_4323 GBV_ILN_4324 GBV_ILN_4325 GBV_ILN_4338 GBV_ILN_4367 GBV_ILN_4700 AR 5 2020 4
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title_full	Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in <italic toggle="yes"<Rhizobiales</italic<
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author_browse	Sishuo Wang Andrew Meade Hon-Ming Lam Haiwei Luo
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title_sort	evolutionary timeline and genomic plasticity underlying the lifestyle diversity in <italic toggle="yes"<rhizobiales</italic<
callnumber	QR1-502
title_auth	Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in <italic toggle="yes"<Rhizobiales</italic<
abstract	ABSTRACT Members of the order Rhizobiales include those capable of nitrogen fixation in nodules as well as pathogens of animals and plants. This lifestyle diversity has important implications for agricultural and medical research. Leveraging large-scale genomic data, we infer that Rhizobiales originated as a free-living ancestor ∼1,500 million years ago (Mya) and that the later emergence of host-associated lifestyles broadly coincided with the rise of their eukaryotic hosts. In particular, the first nodulating lineage arose from either Azorhizobium or Bradyrhizobium 150 to 80 Mya, a time range in general concurrent with the emergence of legumes. The rates of lifestyle transitions are highly variable; nodule association is more likely to be lost than gained, whereas animal association likely represents an evolutionary dead end. We searched for statistical correlations between gene presence and lifestyle and identified genes likely contributing to the transition and adaptation to the same lifestyle in divergent lineages. Among the genes potentially promoting successful transitions to major nodulation lineages, the nod and nif clusters for nodulation and nitrogen fixation, respectively, were repeatedly acquired during each transition; the fix, dct, and phb clusters involved in energy conservation under micro-oxic conditions were present in the nonnodulating ancestors; and the secretion systems were acquired in lineage-specific patterns. Our study data suggest that increased eukaryote diversity drives lifestyle diversification of bacteria and highlight both acquired and preexisting traits facilitating the origin of host association. IMPORTANCE Bacteria form diverse interactions with eukaryotic hosts. This is well represented by the Rhizobiales, a clade of Alphaproteobacteria strategically important for their large diversity of lifestyles with implications for agricultural and medical research. To investigate their lifestyle evolution, we compiled a comprehensive data set of genomes and lifestyle information for over 1,000 Rhizobiales genomes. We show that the origins of major host-associated lineages in Rhizobiales broadly coincided with the emergences of their host plants/animals, suggesting bacterium-host interactions as a driving force in the evolution of Rhizobiales. We further found that, in addition to gene gains, preexisting traits and recurrent losses of specific genomic traits may have played underrecognized roles in the origin of host-associated lineages, providing clues to genetic engineering of microbial agricultural inoculants and prevention of the emergence of potential plant/animal pathogens.
abstractGer	ABSTRACT Members of the order Rhizobiales include those capable of nitrogen fixation in nodules as well as pathogens of animals and plants. This lifestyle diversity has important implications for agricultural and medical research. Leveraging large-scale genomic data, we infer that Rhizobiales originated as a free-living ancestor ∼1,500 million years ago (Mya) and that the later emergence of host-associated lifestyles broadly coincided with the rise of their eukaryotic hosts. In particular, the first nodulating lineage arose from either Azorhizobium or Bradyrhizobium 150 to 80 Mya, a time range in general concurrent with the emergence of legumes. The rates of lifestyle transitions are highly variable; nodule association is more likely to be lost than gained, whereas animal association likely represents an evolutionary dead end. We searched for statistical correlations between gene presence and lifestyle and identified genes likely contributing to the transition and adaptation to the same lifestyle in divergent lineages. Among the genes potentially promoting successful transitions to major nodulation lineages, the nod and nif clusters for nodulation and nitrogen fixation, respectively, were repeatedly acquired during each transition; the fix, dct, and phb clusters involved in energy conservation under micro-oxic conditions were present in the nonnodulating ancestors; and the secretion systems were acquired in lineage-specific patterns. Our study data suggest that increased eukaryote diversity drives lifestyle diversification of bacteria and highlight both acquired and preexisting traits facilitating the origin of host association. IMPORTANCE Bacteria form diverse interactions with eukaryotic hosts. This is well represented by the Rhizobiales, a clade of Alphaproteobacteria strategically important for their large diversity of lifestyles with implications for agricultural and medical research. To investigate their lifestyle evolution, we compiled a comprehensive data set of genomes and lifestyle information for over 1,000 Rhizobiales genomes. We show that the origins of major host-associated lineages in Rhizobiales broadly coincided with the emergences of their host plants/animals, suggesting bacterium-host interactions as a driving force in the evolution of Rhizobiales. We further found that, in addition to gene gains, preexisting traits and recurrent losses of specific genomic traits may have played underrecognized roles in the origin of host-associated lineages, providing clues to genetic engineering of microbial agricultural inoculants and prevention of the emergence of potential plant/animal pathogens.
abstract_unstemmed	ABSTRACT Members of the order Rhizobiales include those capable of nitrogen fixation in nodules as well as pathogens of animals and plants. This lifestyle diversity has important implications for agricultural and medical research. Leveraging large-scale genomic data, we infer that Rhizobiales originated as a free-living ancestor ∼1,500 million years ago (Mya) and that the later emergence of host-associated lifestyles broadly coincided with the rise of their eukaryotic hosts. In particular, the first nodulating lineage arose from either Azorhizobium or Bradyrhizobium 150 to 80 Mya, a time range in general concurrent with the emergence of legumes. The rates of lifestyle transitions are highly variable; nodule association is more likely to be lost than gained, whereas animal association likely represents an evolutionary dead end. We searched for statistical correlations between gene presence and lifestyle and identified genes likely contributing to the transition and adaptation to the same lifestyle in divergent lineages. Among the genes potentially promoting successful transitions to major nodulation lineages, the nod and nif clusters for nodulation and nitrogen fixation, respectively, were repeatedly acquired during each transition; the fix, dct, and phb clusters involved in energy conservation under micro-oxic conditions were present in the nonnodulating ancestors; and the secretion systems were acquired in lineage-specific patterns. Our study data suggest that increased eukaryote diversity drives lifestyle diversification of bacteria and highlight both acquired and preexisting traits facilitating the origin of host association. IMPORTANCE Bacteria form diverse interactions with eukaryotic hosts. This is well represented by the Rhizobiales, a clade of Alphaproteobacteria strategically important for their large diversity of lifestyles with implications for agricultural and medical research. To investigate their lifestyle evolution, we compiled a comprehensive data set of genomes and lifestyle information for over 1,000 Rhizobiales genomes. We show that the origins of major host-associated lineages in Rhizobiales broadly coincided with the emergences of their host plants/animals, suggesting bacterium-host interactions as a driving force in the evolution of Rhizobiales. We further found that, in addition to gene gains, preexisting traits and recurrent losses of specific genomic traits may have played underrecognized roles in the origin of host-associated lineages, providing clues to genetic engineering of microbial agricultural inoculants and prevention of the emergence of potential plant/animal pathogens.
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title_short	Evolutionary Timeline and Genomic Plasticity Underlying the Lifestyle Diversity in <italic toggle="yes"<Rhizobiales</italic<
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